Biology and Worldwide Situation of Diaphorina citri Kuwayama,

Biology and Worldwide Situation

of Diaphorina citri Kuwayama,

1908 (Hemiptera: Liviidae)

M. Setamou

Texas A&M University-Kingsville

[email protected]

Outline

� Nomenclature

� Geographic origin and current distribution

� Origin of D. citri present in the Americas

� Description, Life cycle and Biology

Host plants� Host plants

� Factors affecting D. citri biology (preference and

development) and population growth

� Behavior and spatio-temporal distribution

� CLas acquisition and transmission by D. citri

Diaphorina citri Kuwayama, 1908

Kuwayama Sh. 1908 - Die Psylliden Japans. I. Transactions of the

Sapporo Natural History Society 2: 149-189 [160].

Common Name: Asian citrus psyllid (ACP)

Diaphorina citri Kuwayama, 1908

� Liviidae Löw, 1879

� Euphyllurinae Crawford, 1914

� Diaphorina Löw, 1880Löw F. 1880 - Mittheilungen über Psylloden. Verhandlungen der Zoologischbotanischen Gesellschaft in Wien 29: 549-598 [567]

SynonymsSynonyms

� Diaphora Löw, 1879

� Gonanoplicus Enderlein, 1910

� Pennavena Capener, 1968

� Eudiaphorina Loginova, 1975

� Brachypsylla Froggatt, 1901

Geographic origin of D. citri

� South-western Asia (Halbert & Manjunath 2004, Beattie et al. 2009)

� ACP has evolved in India (Beattie et al. 2009)

� In Asia: China, India, Myanmar, Taiwan, Phillippine Islands,

Malaysia, Indonesia, Sri Lanka, Pakistan, Thailand, Nepal, Ryukyu

Islands (Japan), Afghanistan, Saudi Arabia, Reunion, and MauritiusIslands (Japan), Afghanistan, Saudi Arabia, Reunion, and Mauritius

� Americas: Most of South, North and Central American countries

� In the USA: FL (1998), TX (2001), CA (2008), but also present in AZ,

LA, AL, GA, MS and SC

1990s

1940s

Geographic origin: Southwestern Asia, “India”

Ouvrard, D. (2013) Psyl'list - The World Psylloidea Database. http://www.hemiptera

databases.com/psyllist - searched on 15 August 2013

1940sBrazil

Argentina

Venezuela

Network of evolutionary relationships among COI

haplotypes of D. citri in the Americas and Hawaii

� 23 haplotypes

identified that fell

into two groups

� hp1 present in

highest frequency in

group1

De Leon et al. 2011, Annals of Entomological

Society of America 104: 1392-1398.

group1

� hp9 present in

highest frequency in

group 2

� No hp shared

between the 2 groups

� (ΦCT=0.733; P<0.001)

Network of genealogical relationships among COI

haplotypes of D. citri in the Americas and Hawaii

� ParsimonySplits and

Statistical Parsimony

discriminated 2

groups

hp1 & hp9 considered � hp1 & hp9 considered

ancestral haplotypes

� In each group all

other hp derived from

them

Two founding events of D. citri in the Americas

Phylogenetic relationships between worldwide population of ACP

SWA

Haplotype network generated with statistical parsimony analysis of D. citri mtCOIDNAsequence

(Boykin et al. 2012, Bulletin of Entomological Research 102: 573-582

SEA

Two founding events of D. citri in the Americas and

Hawaii

Major Group Countries Haplotype

group

South

America

Argentina, Brazil,

Paraguay, Uruguay

Southeastern

Asia

North &

Central

America

Belize, Costa Rica, Hawaii,

Mexico, and USA

(California, Florida and

Texas)

Southwestern

Asia

Both haplotype groups invaded separate locations of Brazil.

Haplotype unique to the Caribbean (Puerto Rico & Guadeloupe)

was also found (Boykin et al. 2012)

World distribution of D. citri in the Americas

D. citri in Hawaii

D. citri in Asia

3000 m

Distribution of (1) Heat tolerant Asian psyllid, Diaphorina citri, and (2) Heat sensitive

African psyllid, Trioza erytreae, in Reunion island

3000 m

Diaphorina citri Trioza erytreae

: below ~500m: above ~500m

Description, life cycle and biology of ACP

Diaphorina citri-Adult

� Small (2.7-3.3 mm long) with

mottled brown wings

� 3 abdominal colors (gray/brown,

blue/green, orange/yellow)

� Gravid females are mostly

First reported in Florida in June 1998

& in Texas in September 2001, by 2008,

several states in the U.S.

� Gravid females are mostly

orange/yellow but significant of

colors remain largely unknown

� Sex ratio is ca. 1:1

� Adult feeding position is 30-45° from

plant surface

Diaphorina citri-Adult

Feeding sites of adults Trees flushing No new flush

Young shoots 49.5 A -

Midrib/veins of leaf 24.0 B 38.5 a

Leaf margin 13.0 C 43.0 a

Twig 13.5 C 18.5 b

Chi-square 8.32 * 25.44***

Diaphorina citri-Adult� Adult locate their mates using vibrational sounds,

and females emitted pheromones

� Adults mate multiple times

� ACP is a diurnal insect: Mating, oviposition,

movement restricted to daytime (light is

important)

� Female lay eggs throughout life time only if

First reported in Florida in June 1998

& in Texas in September 2001, by 2008,

several states in the U.S.

� Female lay eggs throughout life time only if

young shoots are present (500-1,000 eggs)

� Reproductive maturity reached in 2-3d after

emergence

� Egg laying begin 1-2d after mating

� Adult live 2-3 months, but longevity is host plant,

temperature and RH dependent

ACP Eggs� Almond-shaped eggs

� Bright-yellow in color when

freshly deposited but turn

orange when mature with 2

visible red eye spots

Laid on the tips of new flushes � Laid on the tips of new flushes

or in crevices of unopened

leaves

� Fixed to the site by a small stalk

driven into the tissue called

pedicel (moisture driven)

Psyllid Nymphs

� Eggs hatch into small nymphs that go thru 5

instars (gradual metamorphosis)

� Flat, yellow-orange (0.01-0.07 inch)

� 2 red eye-spots that can be seen from 2nd

instar

� Wing pad from the 3rd instar� Wing pad from the 3 instar

� Settle and start feeding after hatching, but 2nd

instar move to young stems

� Produce honeydew and waxy tubules that

direct the honeydew

� Nymphal development takes 10 to 21 days; 16

d at 25°C

D. citri development� Oviposition and development are temperature and

humidity dependent

� Egg laying occurs between 16-42°C, w/ peaks at 25-

30°C

� Very few eggs laid when RH < 40%

� Developmental time from egg to adult ranged from

14.1d at 28°C to 49.3 at 15°C with optimum temp 14.1d at 28°C to 49.3 at 15°C with optimum temp

at 24-28°C

� Generation time is 20-22d at 25°C

� ACP overwinters as adult in citrus

� Adults and nymphs can survive at -8 to -6°C for

several hrs. Mild to moderate freeze events are

non-lethal to ACP, but may lower spring pop.

D. citri feeding

� ACP adults and nymphs have piercing-sucking

mouthparts, feed by inserting stylet into

phloem tissue leaving their salivary sheaths and

stylet tracks behind

� Adults found on young stems and leaves of all

ages while nymphs only found on young leaves

and stems (shoots)and stems (shoots)

� Nymphs produce tube-like waste covered by

waxy white materials

� Adult females also produce waxy excretory

substance but males produce clear substance

D. Citri life cycle

11-39 d2.6-8.2 d

13.3-47.5 d

D. citri host plants� ACP is an oligophagous with host plants restricted to

the Rutaceae family, sub-family Aurantioideae (Citrus

and relatives)

� A Moraceae (Ficus carica L.) has been reported as hosts

by Thomas & De Leon (2011), but we did not confirm

these findingsthese findings

� Within its host plant family, ACP exhibit strong host

plant preference which affects its oviposition,

development, longevity, reproduction and size

(morphometric analysis)

� Larger adults recorded on preferred hosts (e.g. Lemon)

D. citri host plants� Most species in the genus Citrus are common hosts but there is huge

variation in the preference/performance of ACP on these hosts

� Plants in other genera are also recorded as host plants of ACP:

Bergera koenigii, Murraya exotica & M. paniculata, Microcitrus sp.,

Alatantia sp., Eremocitrus glauca, Fortunella spp., Merrillia

caloxylon, Zanthoxylum fagara, Poncirus trifoliata, Choisya ternata,

C. arizonica, and Helietta barettaC. arizonica, and Helietta baretta

� Other Rutacae are just egg laying sites in no-choice situations but do

not support nymphal development (Amyris madrensis, A. texana,

Zanthoxylum clavahercules)

� Some Rutaceae are known non-host species (Esenbeckia berlandieri,

Ptelea trifoliata, Casimiroa tetrameria, C. edulis, Sargentia greggii)

D. citri host plants� Reason of acceptance of some Rutaceae and non-

acceptance of others as host plants is poorly understood

� What we do know is that on yellow chapote (Casimiroa

greggii) the presence of hairs does not allow successful

establishment of nymphs for feeding although adult

survival and egg laying occursurvival and egg laying occur

� Elucidating this will help in developing resistance

materials to ACP

� Among the known host plants, ACP exhibit strong host

plant preference

D. citri preferred host plants

Bergera koenigii(curry leaf plant)

Murraya(orange jasmine)

Microcitrus(finger lime)(curry leaf plant) (orange jasmine) (finger lime)

Citrus limon(lemon)

Citrus aurantifolia(lime)

Citrus sinensis(sweet orange)

D. citri host preference

� Psyllid choice arena (PCA) used in D. citri host preference

study (8 host plants can be used simultaneously)

D. citri host preferenceM

ean

Ran

k

4

6

8

a(10)

ab(3) abc

(3) bcd(4)

bcd(3) cd

(2)d(1)

Values in parenthesis depict the number of first choices for each

Valley

Lem

onTa

nger

ineVale

ncia

Rio Red

Mexica

n Lim

e

Orang

e Ja

smine

Yellow

Cha

pote

Blank

0

2 e(0)

first choices for each host plant

Factors governing D. citri host plant selection

� Combination of visual, olfactory, tissue softness and

nutritive value of flush shoots

� Visual characteristic (higher reflectance values in the

yellow range)

� Olfactory cues (some sesquiterpenes involve in ACP � Olfactory cues (some sesquiterpenes involve in ACP

adult attraction)

� Tissue softness allowing copious feeding and egg laying

� Nutrient content of flush shoot (high N and protein

content)

Flush shoot growth stages and ACP phenology

I II III IV VI II III IV V

Eggs

Nymphs

Adults

Spectral reflectance of citrus flush shoots

(sweet orange)

�Stage 1 �Stage 2 �Stage 3 �Stage 4 �Stage 5

Spectral reflectance of citrus flush shoots

(Grapefruit)

�Stage 1 �Stage 2 �Stage 3 �Stage 4 �Stage 5

2.50E+02

3.00E+02

3.50E+02

4.00E+02

Close Bud2

Breaking BudClose2

CloseFeatherFlush2

2.5closeupper1

4.0closeupper1

Factors governing D. citri host plant selection:

Flush shoot reflectance

0.00E+00

5.00E+01

1.00E+02

1.50E+02

2.00E+02

346

364

382

400

418

436

454

472

490

508

526

544

562

580

598

616

634

652

670

688

706

724

742

760

778

796

814

832

850

868

886

904

922

940

958

976

994

1012

1030

1048

1066

1084

4.0closeupper1

5.0closeupper1

NewLeafClose1

FullyExpandedSoft CloseUpper1MatureCloseUpper12

Volatile profile of flush shoot

Young flush shoot Mature flush shoot

Orange jasmine

Volatile profile of flush shoot

� Young flush

shoot

� Mature flush shoot

Kaffir lime


Flush shoot architecture


Flush nutrient content

3

4

5

0

1

2

3

1 2 3 4 5

(%)

Flush developmental stage

N

Ca


Flush shoot C:N Ratio

20.00(%

)

0.00

10.00

1 2 3 4 5C:N ratio 12.38 14.89 15.81 16.33 18.32

(%)

Eggs are deposited on soft tissue-As flush shoots mature


Tissue softness

� Eggs are deposited on soft tissue-As flush shoots mature

their softness decreases. Good relationship between

tissue softness and number of eggs laid

� Flush shoot availability, softness and speed of maturity

could explain differenSal densiSes of ACP on ≠host plants

(lemon shoots are soft, lime & lemon frequent flushing)

� In citrus groves, ACP population is intimately related to

flush cycles because egg laying and nymphal

development ONLY occur on young shoots

� Host species also determine ACP population

� Periods of peak ACP populations depend on the region:

E.g. in Florida large ACP infestations occur from late

Factors governing D. citri populations

E.g. in Florida large ACP infestations occur from late

Spring to mid-Summer, in contrast in Texas, ACP

populations gradually increased reaching its peak in

September (late Summer to Fall)


D.

citr

i a

du

lts/

flu

sh s

ho

ot

2

3

4

Grapefruit

OrangeMajor flushing periods

2009

Feb

Mar

Apr M

ay

Jun Ju

l Aug

Se

p O

ct

Nov

Dec

Ja

n Fe

b N

um

be

rs o

f D

. ci

tri

0

1

� Adult numbers increased with new flush shoots

ny

mp

hs/

flu

sh s

ho

ot

12

14

16

Grapefruit

Orange

M ajor flushing periods


Immatures only present when new flush are produced

2009

Feb M

ar A

pr M

ay Ju

n

Jul

Aug Sep O

ct

Nov D

ec

Jan

Feb N

um

be

rs o

f D

. ci

tri

ny

mp

hs/

flu

sh s

ho

ot

0

2

4

6

8

10

� ACP is a weak flyer: Adults cannot fly very far or sustain

long flights because of weak muscles relative to large size

of wings

� Longest flight is 47-49 minutes in flight mill (Arakawa & Mivamolo 2007)

� Longest distance is 978m for females and 1.2 km for

males (speed 1.4 km/hr)

ACP flight behavior

males (speed 1.4 km/hr)

� ACP active during daytime

� ACP can be transported by winds over long distance

� However due to its posture, ACP adults mostly face the

direction where wind is coming from: explain higher

densities on southeast of groves in FL & TX (dominant wind SE)

� ACP are frequent movers, move frequently between

adjacent groves, thus explaining the border effects in

ACP spatial distribution in the field

� Studies need to be conducted within each region to

determine which side of the grove is the most infested

Field distribution

Field distribution studies of D. citri

Border Adjacent Interior

� Strong edge effects

in the distribution

of ACP that could

be used for

developing control

methods

Field distribution

10

20

30

40

50PerimeterAdjacentInterior

Mea

n A

CP

Adults

/ Tra

p

Young Trees

methods 0

Date (2012)

Feb Apr Jun Aug Oct

Mea

n A

CP

Adults

/ Tra

p

0.0

0.2

0.4

0.6

0.8

1.0

Mature Trees

� Strong edge effects

in the distribution

of ACP that could

be used for

developing control

methods

Field distribution

2

4

6

8

Per

cen

tag

e F

lush

Infe

sted

Grapefruit

y = 4.51*exp(-0.0210*x)

methods0

Distance of Tree Location from Perimeter (m)

0 10 20 30 40

Per

cen

tag

e F

lush

Infe

sted

0

2

4

6

8Orange

y = 6.89*exp(-0.0235*x)

Field distribution

01

02

03

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05

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09

10

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7596600

90

95

100

105

90 97

98

99

778200 778250 778300 778350 778400 778450 778500 778550

Longitude (UTM)

7596250

7596300

7596350

7596400

7596450

7596500

7596550

Latit

ude

(UTM

)

15

20

25

30

35

40

45

50

55

60

65

70

75

80

85

90

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� Monitoring of ACP:

� visual observations (for immatures)

� tap sampling (beat sheets, bucket)

� Sticky traps (yellow & lime-green)

ACP Monitoring

� Sticky traps (yellow & lime-green)

� Sweep nets & vacuum

� Choice of method depends on objectives of

study

CLas acquisition and transmission by ACP

Summary� ACP from India, 2 founding events in America

� ACP in North America from southwestern Asia

� ACP exhibit strong host plant preference: Lime, Lemon

>> Sweet oranges >> Grapefruit

� Population fluctuations depend on flush cycles

Border effects on ACP distribution� Border effects on ACP distribution

� Frequent movement of ACP between groves

� Spatio-temporal behavior of ACP dictates AWM

strategies for ACP

� Acquisition of CLas greatest at nymphal stage (management strategies should prevent nymphal development)

Dr. De Leon, USDA

Dr. David Hall, USDA Fort Pierce

Dr L. Stelinski, UF

Dr. Pelz-Stelinski, UF

Dr. M. Rogers

Acknowledgments

Dr. M. Rogers

Dr. P. Yamamoto Univ of Sao Paolo

TX Citrus Growers

THANK YOU!

GRACIASGRACIAS

Biology and Worldwide Situation of Diaphorina citri Kuwayama,

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Transcript of Biology and Worldwide Situation of Diaphorina citri Kuwayama,